Activated microglia in nociception

Pain Physician

Volumn 13, Issue 3, 2010, Pages 295-304

  Smith, Howard S ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

Author keywords

C fiber nociceptors; Glia; Hyperplasia; Hypertrophy; Microglial cells; Neuropathic pain

Indexed keywords

17 DEMETHOXY 17 (2 DIMETHYLAMINOETHYLAMINO)GELDANAMYCIN; BICUCULLINE; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CX3CR1; ECHISTATIN; FRACTALKINE; GAMMA INTERFERON; GAMMA INTERFERON RECEPTOR; GELDANAMYCIN; MATRIX METALLOPROTEINASE; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; OMEGA 3 FATTY ACID; PURINERGIC P2X4 RECEPTOR; TOLL LIKE RECEPTOR 4;

ALLODYNIA; ANALGESIC ACTIVITY; ARTICLE; CELL ACTIVATION; DRUG TARGETING; ENZYME INHIBITION; GLIA CELL; HUMAN; HYPERPLASIA; HYPERTROPHY; MICROGLIA; NERVE CELL LESION; NEUROPATHIC PAIN; NOCICEPTION; NOCICEPTIVE RECEPTOR; NONHUMAN; SIGNAL TRANSDUCTION;

ANIMALS; CHEMOKINE CCL2; CHEMOKINE CX3CL1; HUMANS; HYPERPLASIA; HYPERTROPHY; INTERFERON-GAMMA; MICROGLIA; NEURALGIA; NEUROPEPTIDES; NOCICEPTORS; RECEPTORS, PURINERGIC P2; SPINAL CORD; TOLL-LIKE RECEPTOR 4;

EID: 77953334827     PISSN: 15333159     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (80)

1. Ji RR, Strichartz G. Cell signaling and the genesis of neuropathic pain. Sci STKE 2004; 252:reE14.
2. McMahon SB, Cafferty WB, Marchand F. Immune and glial cell factors as pain mediators and modulators. Exp Neurol 2005; 192:444-462.
3. Tsuda M, Inoue K, Salter MW. Neuropathic pain and spinal microglia: A big problem from molecules in "small" glia. Trends Neurosci 2005; 28:101-107.
4. Milligan ED, Watkins LR. Pathological and protective roles of glia in chronic pain. Nat Rev Neurosco 2009; 10:23-36.
5. Watkins LR, Milligan ED, Maier SF. Glial activation: A driving force for pathological pain. Trends Neurosci 2001; 24:450-455.
6. Sommer C. Painful neuropathies. Curr Opin Neurol 2003; 16:623-628.
7. Watkins LR, Maier SF. Glia: A novel drug discovery target for clinical pain. Nat Rev Drug Discov 2003; 2:973-985.
8. Hathway GJ, Vega-Avelaira D, Moss A, Ingram R, Fitzgerald M. Brief, low frequency stimulation of rat peripheral C-fibers evokes prolonged microglial-induced central sensitization in adults but not in neonates. Pain 2009; 144:110-118.
9. Fu KY, Light AR, Maixner W. Relationship between nociceptor activity, peripheral edema, spinal microglial activation in cutaneous hyperalgesia. Pain 2000; 101:1127-1135.
10. Sun S, Cao H, Han M, Li TT, Pan HL, Zhao ZQ, Zhang YQ. New evidence for the involvement of spinal fractalkine receptor in pain facilitation and spinal glial activation in rat model of monoarthritis. Pain 2007; 129:64-75.
11. Romero-Sandoval A, Chai N, Nutile-Mc-Menemy N, Deleo JA. A comparison of spinal lba 1 and GFAP expression in rodent models of acute and chronic pain. Brain Res 2008; 1219:116-126.
12. Kawasaki Y, Xu ZZ, Wang X, Park JY, Zhuang ZY, Tan PH, Gao YJ, Roy K, Corfas G, Lo EH, Ji RR. Distinct roles of atrix metalloproteases in the early- and late-phase development of neuropathic pain. Nat Med 2008; 14:331-336.
13. Tanga FY, Raghavendra V, Deleo JA. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain Neurochem Int 2004; 45:397-407.
14. Scholtz J, Wollf CJ. The neuropathic pain triad: Neurons, immune cells and glia. Nat Neurosci 2007; 10:1361-1368.
15. Zhuang ZY, Gerner P, Woolf CJ, Ji RR. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in the neuropathic pain model. Pain 2005; 114:149-159.
16. Suter MR, Wen YR, Decosterd I, Ji RR. Do glial cells control pain? Neuron Glia Biol 2007; 3:255-268.
17. Zhuang ZY, Kawasaki Y, Tan PH, Wen YR, Huang J, Ji RR. Role of the CX3CR1/p38 MAPK pathway in spinal microglia for the development of neuropathic pain following nerve injury-induced cleavage of fractalkine. Brain Behav Immun 2007; 21:642-651.
18. Kim D, Kim MA, Cho IH, Kim MS, Lee S, Jo EK, Choi SY, Park K, Kim JS, Akira S, Na HS, Oh SB, Lee SJ. A critical role of toll- like receptor 2 in nerve injury-induced spinal cord glial cell activation and pain hypersensitivity. J Biol Chem 2007; 282:14975-14983.
19. Kobayashi K, Yamanaka H, Fukuoka T, Dai Y, Obata K, Noguchi K. P2Y12 receptor upregulation in activated microglia is a gateway of p38 signaling and neuropathic pain. J Neurosci 2008; 28:2892-2902.
20. Obata K, Katsura H, Miyoshi K, Kondo T, Yamanaka H, Kobayashi K, Dai Y, Fukuoka T, Akira S, Noguchi K. Toll-like receptor 3 contributes to spinal glial activation and tactile allodynia after nerve injury. J Neurochem 2008; 105:2249-2259.
21. Kobayashi H, Chattopadhyay S, Kato K, Dolkas J, Kikuchi S, Myers RR, Shubayev VI. MMPs initiate Schwann cellmediated MBP degradation and mechanical nociception after nerve damage. Mol Cell Neurosci 2008; 39:619-627.
22. Liuzzi GM, Latronico T, Rossano R, Viggiani S, Fasano A, Riccio P. Inhibitory effect of polyunsaturated fatty acids on MMP-9 release from microglial cells---implications for complementary multiple sclerosis treatment. Neurochem Res 2007; 32:2184-2193.
23. Liu G, Bibus DM, Bode AM, Ma YY, Holman RT, Dong Z. Omega 3 but not omega 6 fatty acids inhibit AP-1 activity and cell transformation in JB6 cells. Proc Natl Acad Sci USA 2001; 98:7510-7515.
24. van den Steen PE, Dubois B, Nelissen I, Rudd PM, Dwek RA, Opdenakker G. Biochemistry and molecular biology of gelatinase B or matrix metalloproteinase-9 (MMP-9). Crit Rev Biochem Mol Biol 2002; 37:375-536.
25. Inoue K, Tsuda M. Microglia and Neuropathic Pain. Glia 2009; 57:1469-1479.
26. Kreutzberg GW. Microglia: A sensro for pathological events in the CNS. Trends Neurosci 1996; 19:312:318.
27. Raivich G, Bohatschek M, Kloss C, Werner A, Jones LL, Kreutzberg GW. Neuroglial activation repertoire in the injured brain: Graded response, molecular mechanisms and cues to physiological function. Brain Res Brain Res Rev 1999; 30:77-105.
28. Beggs S, Salter MW. Stereological and somatotopic analysis of the spinal microglial response to peripheral nerve injury. Brain Behav Immun 2007; 21:624-633.
29. Clark AK, Yip PK, Grist J, Gentry C, Staniland AA, Marchand F, Dehvari M, Wotherspoon G, Winter J, Ullah J, Bevan S, Malcangio M. Inhibition of spinal microglial cathepsin S for the reversal of neuropathic pain. Proc Natl Acad Sci USA 2007; 104:10655-10660.
30. Thacker MA, Clark AK, Bishop T, Grist J, Yip PK, Moon LD, Thompson SW, Marchand F, McMahon SB. CCL2 is a key mediator of microglia activation in neuropathic pain states. Eur J Pain 2009; 13:263-272.
31. 4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003; 424:778-783.
32. Zhang J, Shi XQ, Echeverry S, Mogil JS, De Koninck Y, Rivest S. Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J Neurosci 2007; 27:12396-12406.
33. Jin SX, Zhuang ZY, Woolf CJ, Ji RR. p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci 2003; 23:4017-4022.
34. Tsuda M, Mizokoshi A, Shigemoto-Mogami Y, Koizumi S, Inoue K. Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury. Glia 2004; 45:89-95.
35. Clark AK, Yip PK, Malcangio M. The liberation of fractalkine in the dorsal horn requires microglial cathepsin S. J Neurosci. 2009; 29:6945-6954.
36. Ceyhan GO, Deucker S, Demir IE, Erkan M, Schmelz M, Bergmann F, Müller MW, Giese T, Büchler MW, Giese NA, Friess H. Neural fractalkine expression is closely linked to pain and pancreatic neuritis in human chronic pancreatitis. Lan Invest 2009; 89:347-361.
37. Tsuda M, Masuda T, Kitano J, Shimoyama H, Tozaki-Saitoh H, Inoue K. IFNgamma receptor signaling mediates spinal microglia activation driving neuropathic pain. Proc Natl Acad Sci USA 2009; 106:8032-8037.
38. Tanaka T, Minami M, Nakagawa T, Satoh M. Enhanced production of monocyte chemoattractant protein-1 in the dorsal root ganglia in a rat model of neuropathic pain: Possible involvement in the development of neuropathic pain. Neurosci Res 2004; 48:463-469.
39. White FA, Sun J, Waters SM, Ma C, Ren D, Ripsch M, Steflik J, Cortright DN, Lamotte RH, Miller RJ. Excitatory monocyte chemoattractant protein-1 signaling is up-regulated in sensory neurons after chronic compression of the dorsal root ganglion. Proc Natl Acad Sci USA 2005; 102:14092-14097.
40. Zhang J, De Koninck Y. Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury. J Neurochem 2006; 97:772-783.
41. Zhang J, Shi XQ, Echeverry S, Mogil JS, De Koninck Y, Rivest S. Expression of CCR2 in both resident and bone marrow-derived microglia plays a critical role in neuropathic pain. J Neurosci 2007; 27:12396-12406.
42. Peters CM, Eisenach JC. Contribution of the chemokine (C-C motif) ligand 2 (CCL2) to mechanical hypersensitivity after surgical incision in rats. Anesthesiology 2010; 112:1250-1258.
43. Dansereau MA, Goddelin RD, Pohl M, Pommier B, Mechighel P, Mauborgne A, Rostene W, Kitabgi P, Beaudet N, Sarret P, Melik-Parsadaniantz S. Spinal CCL2 pronocicpetive action is no longer effective in CCR2 receptor antagonists-treated rats. J Neurochem 2008; 106:757-769.
44. Jung H, Toth PT, White FA, Miller RJ. Monocyte chemoattractant protein-1 functions as a neuromodulator in dorsal root ganglia neurons. J Neurchem 2008; 104:254-263.
45. Chen Y, Willcockson HH, Valtschanoff JG. Influence of the vanilloid receptor TRPV1 on the activation of spinal cord glia in mouse models of pain. Exp Neurol 2009; 220:383-390.
46. Uematsu S, Akira S. Toll-like receptors and innate immunity. J Mol Med 2006; 84:712-725.
47. Kawai T, Akira S. Signaling to NF-kappaB by Toll-like receptors. Trends Mol Med 2007; 13:460-469.
48. Laflamme N, Rivest S. Toll-like receptor 4: the missing link of the cerebral innate immune response triggered by circulating gram-negative bacterial cell wall components. FASEB J 2001; 15:155-163.
49. Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, Hagberg H. Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 2001; 13:1101-1106.
50. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, Jensen FE, Rosenberg PA,Volpe JJ, Vartanian T. The tolllike receptor TLR4 is necessary for lipopolysaccharide-induced oligodendrocyte injury in the CNS. J Neurosci 2002; 22:2478-2486.
51. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, Volpe JJ, Vartanian T. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci USA 2003; 100:8514-8519.
52. Vabulas RM, Ahmad-Nejad P, Ghose S, Kirschning CJ, Issels RD, Wagner H. HSP70 as endogenous stimulus of the Toll/interleukin-1 receptor signal pathway. J Biol Chem 2002; 277:15107-15112.
53. Tsan MF, Gao B. Cytokine function of heat shock proteins. Am J Physiol 2004; 286:C739-C744.
54. Tanga FY, Raghavendra V, DeLeo JA. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain. Neurochem Int 2004; 45:397-407.
55. Tanga FY, Nutile-McMenemy N, DeLeo JA. The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci U S A 2005; 102:5856-5861.
56. Bettoni I, Comelli F, Rossini C, Granucci F, Giagnoni G, Peri F, Costa B. Glial TLR4 receptor as new target to treat neuropathic pain: Efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice. Glia 2008; 56:1312-1319.
57. Hutchinson MR, Ramos KM, Loram LC, Wieseler J, Sholar PW, Kearney JJ, Lewis MT, Crysdale NY, Zhang Y, Harrison JA, Maier SF, Rice KC, Watkins LR. Evidence for a role of heat shock protein-90 in Toll like receptor 4 mediated pain enhancement in rats. Neurosci 2009; 164:1821-1832.
58. Burnstock G. Purinergic nerves. Pharmacol Rec 1972; 24:509-581.
59. Burnstock G. Purinergic signaling and disorders of the central nervous system. Nat Rev Drug Discov 2008; 7:575-590.
60. Lewis C, Neidhart S, Holy C, North RA, Buell G, Surprenant A. Coexpression of P2X2 and P2X3 receptor subunits can account for ATP-gated currents in sensory neurons. Nature 1995; 377:432-435.
61. Chen CC, Akopian AN, Sivilotti L, Colquhoun D, Burnstock G, Wood JN. A P2X purinoceptor expressed by a subset of sensory neurons. Nature 1995; 377:428-431.
62. Donnelly-Roberts D, McGaraughty S, Shieh CC, Honore P, Jarvis MF. Painful purinergic receptors. J Pharmacol Exp Ther 2008; 324:409-415.
63. Kennedy C, Assis TS, Currie AJ, Rowan EG. Crossing the pain barrier: P2 receptors as targets for novel analgesics. J Physiol 2003; 553:683-694.
64. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 2007; 87:659-797.
65. Khakh BS, Burnstock G, Kennedy C, King BF, North RA, Seguela P, Voigt M, Humphrey PP. International union of pharmacology. XXIV. Current status of the nomenclature and properties of P2X receptors and their subunits. Pharmacol Rev 2001; 53:107-118.
66. North RA. Molecular physiology of P2X receptors. Physiol Rev 2002; 82:1013-1067.
67. Fields RD, Burnstock G. Purinergic signaling in neuron-glia interactions. Nat Rev Neurosci 2006; 7:423-436.
68. Inoue K. Microglial activation by purines and pyrimidines. Glia 2002; 40:156-163.
69. Fujita R, Ma Y, Ueda H. Lysophosphatidic acid-induced membrane ruffling and brain-derived neurotrophic factor gene expression are mediated by ATP release in primary microglia. J Neurochem 2008; 107:152-160.
70. Coull JA, Beggs S, Boudreau D, Boivin D, Tsuda M, Inoue K, Gravel C, Salter MW, De Koninck Y. BDNF from microglia causes the shift in neuronal anion gradient underlying neuropathic pain. Nature 2005; 438:1017-1021.
71. Nasu-Tada K, Koizumi S, Tsuda M, Kunifusa E, Inoue K. Possible involvement of increase in spinal fibronectin following peripheral nerve injury in upregulation of microglial P2X(4), a key molecule for mechanical allodynia. Glia 2006; 53:769-775.
72. Tsuda M, Toyomitsu E, Komatsu T, Masuda T, Kunifusa E, Nasu-Tada K, Koizumi S, Yamamoto K, Ando J, Inoue K. Fibronectin/integrin system is involved in P2X(4) receptor upregulation in thespinal cord and neuropathic pain after nerve injury. Glia 2008; 56:579-585.
73. Pfaff M, McLane MA, Beviglia L, Niewiarowski S, Timpl R. Comparison of disintegrins with limited variation in the RGD loop in their binding to purified integrins alpha IIb beta 3, alpha V beta 3 and alpha 5 beta 1 and in cell adhesion inhibition. Cell Adhes Commun 1994; 2:491-501.
74. Wierzbicka-Patynowski I, Niewiarowski S, Marcinkiewicz C, Calvete JJ, Marcinkiewicz MM, McLane MA. Structural requirements of echistatin for the recognition of alpha(v)beta(3) and alpha(5)beta(1) integrins. J Biol Chem 1999; 274:37809-37814.
75. Kloss CU, Bohatschek M, Kreutzberg GW, Raivich G. Effect of lipopolysaccharide on the morphology and integrin immunoreactivity of ramified microglia in the mouse brain and in cell culture. Exp Neurol 2001; 168:32-46.
76. Milner R, Campbell IL. The extracellular matrix and cytokines regulate microglial integrin expression and activation. J Immunol 2003; 170:3850-3858.
77. Kloss CU, Werner A, Klein MA, Shen J, Menuz K, Probst JC, Kreutzberg GW, Raivich G. Integrin family of cell adhesion molecules in the injured brain: Regulation and cellular localization in the normal and regenerating mouse facial motor nucleus. J Comput Neurol 1999; 411:162-178.
78. Tsuda M, Tozaki-Saitoh H, Masuda T, Toyomitsu E, Tezuka T, Yamamoto T, Inoue K. Lyn tyrosine kinase is required for P2X(4) receptor upregulation and neuropathic pain after peripheral nerve injury. Glia 2008; 56:50-58.
79. Tsuda M, Toyomitsu E, Kometani M, Tozaki-Saitoh H, Inoue K. Mechanisms underlying fibronectin-induced upregulation of P2X4R expression in microglia: Distinct roles of PI3K-Akt and MEKERK signaling pathways. J Cell Mol Med 2009; In press.
80. Tsuda M, Tozaki-Saitoh H, Inoue K. Pain and purinergic signaling. Brain Res Rev 2009; In press.